Juvenile hormone signaling promotes ovulation and maintains egg shape by inducing expression of extracellular matrix genes

Abstract

It is well documented that the juvenile hormone (JH) can function as a gonadotropic hormone that stimulates vitellogenesis by activating the production and uptake of vitellogenin in insects. Here, we describe a phenotype associated with mutations in the Drosophila JH receptor genes, Met and Gce: the accumulation of mature eggs with reduced egg length in the ovary. JH signaling is mainly activated in ovarian muscle cells and induces laminin gene expression in these cells. Meanwhile, JH signaling induces collagen IV gene expression in the adult fat body, from which collagen IV is secreted and deposited onto the ovarian muscles. Laminin locally and collagen IV remotely contribute to the assembly of ovarian muscle extracellular matrix (ECM); moreover, the ECM components are indispensable for ovarian muscle contraction. Furthermore, ovarian muscle contraction externally generates a mechanical force to promote ovulation and maintain egg shape. This work reveals an important mechanism for JH-regulated insect reproduction.

Inter-Alpha-Trypsin Inhibitor Heavy Chain 4 Plays an Important Role in the Development and Reproduction of Nilaparvata lugens

“…The Juvenile hormone (JH) can stimulate vitellogenesis by activating the synthesis and uptake of Vg in N. lugens ; this may serve as the regulatory basis for oocyte maturation [ 31 , 39 ]. Methoprene-tolerant (MeT) is the receptor for JH and is required for the ovarian development of N. lugens [ 40 , 41 ]. In the present study, we detected the expression of N. lugens MeT ( NlMet ) after ds NlITIH4 RNAi.…”

“…The assembly of ovarian muscle ECM may also be affected, and this would cause the decline of ovarian muscle contractility that externally generates a mechanical force to promote ovulation, resulting in difficult ovulation [ 40 ]. Apart from these potential factors, the hydrolysis activities of some proteases, the inflammatory reactions, and immunity related to follicle rupture may also be affected by RNAi.…”

Juvenile Hormone Studies in Drosophila melanogaster

“…Previous studies have shown that incomplete ablation of the CA or mutation of Jhamt results in the reduction of JH level with an associated reduction in fecundity and ovary size ( Gruntenko et al, 2010 ; Wen et al, 2015 ). These reproductive deficiencies are caused by decreases of JH-induced Vg production in the fat body and Vg uptake by the oocytes ( Luo et al, 2021 ) or probably due to reduced germline stem cells ( Luo et al, 2020 ). A recent study reports that the single null mutant of JH receptors, Met 27 or Gce 2 .…”

“…5 K , also shows decreased fecundity but with abnormal egg shape and ovary size gradually increase. Subsequently, a novel mechanism for JH-regulated Drosophila reproduction is uncovered that JH intracellular signaling induces Laminin or Collagen IV gene expressions in ovarian muscle or fat body cells, respectively, which are contributed to the assembly of ovarian muscle extracellular matrix (ECM) that is indispensable for ovarian muscle contraction, then ovarian muscle contraction externally generates a mechanical force to promote ovulation and maintain egg shape ( Luo et al, 2021 ).…”

Juvenile Hormone Synthesis Pathway Gene SfIPPI Regulates Sogatella furcifera Reproduction

“…The juvenile hormone (JH) is a sesquiterpenoid compound synthesized in the corpora allata of insects [1,2]. It is essential for regulating the physiological processes of insect growth, metamorphosis, reproduction, and immunity [3][4][5][6][7][8]. JH biosynthesis is associated with the expression of most JH biosynthetic enzymes in the corpora allata [9].…”